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Cortical Control of Facial Expression

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Cortical Control of Facial Expression Review The Journal of Comparative Neurology Research in Systems Neuroscience DOI 10.1002/cne.23908 Topical review Cortical control of facial expression. René M. Müri1,2,3 1Division of Cognitive and Restorative Neurology, Departments of Neurology and Clinical Research, University Hospital Inselspital, Bern, Switzerland 2Gerontechnology and Rehabilitation Group, University of Bern, Bern, Switzerland 3Center for Cognition, Learning, and Memory, University of Bern, Bern, Switzerland Abbreviated title: Cortical control of facial expression Key words: human, facial expression, emotion, facial innervation | downloaded: 13.3.2017 http://boris.unibe.ch/72088/ This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process which may lead to differences between this version and the Version of Record. Please cite this article as an ‘Accepted Article’, doi: 10.1002/cne.23908 source: © 2015 Wiley Periodicals, Inc. Received: Jan 31, 2015; Revised: Sep 19, 2015; Accepted: Sep 25, 2015 This article is protected by copyright. All rights reserved. Journal of Comparative Neurology Page 4 of 23 Abstract The present topical review deals with the motor control of facial expressions in humans. Facial expressions are a central part of human communication. Emotional face expressions have a crucial role in human non-verbal behavior, allowing a rapid transfer of information between individuals. Facial expressions can be both voluntarily or emotionally controlled. Recent studies in non-human primates and humans revealed that the motor control of facial expressions has a distributed neural representation. At least 5 cortical regions on the medial and lateral aspects of each hemisphere are involved: the primary motor cortex, the ventral lateral premotor cortex, the supplementary motor area on the medial wall, and, finally, the rostral and caudal cingulate cortex. The results of studies in humans and non-human primates suggest that the innervation of the face is bilaterally controlled for the upper part, and mainly contralaterally controlled for the lower part. Furthermore, the primary motor cortex, the ventral lateral premotor cortex, and the supplementary motor area are essential for the voluntary control of facial expressions. In contrast, the cingulate cortical areas are important for emotional expression, since they receive input from different structures of the limbic system. John Wiley & Sons 2 This article is protected by copyright. All rights reserved. Page 5 of 23 Journal of Comparative Neurology Introduction The importance of the human face expression is reflected in art and philosophy since antiquity. Cicero considered facial expressions as “Imago animi vultus” (Cicero, de oratore), the image of the soul. Facial expression was also considered to have prognostic value. For instance, the “facies hippocratica”, or Hippocratic facies, had an empiric, negative prognostic significance, since it indicated that the patient “had moved into the atrium of death.” (Illich, 1995). In humans, the motor nucleus of the facial nerve is the largest of all motor nuclei of the brainstem (Cattaneo and Pavesi, 2014). The comparative anatomy of the facial musculature and of the central nervous apparatus that controls facial movements suggest that, in some primates, group size, facial motor control, and primary visual cortex evolved with the same pattern (Dobson & Sherwood, 2011). Species living in relatively large social groups tend to have relatively large facial motor nuclei, and species with enlarged facial nuclei and facial mobility have rather large primary visual cortices (Dobson, 2009; Barton, 1998). Great apes and humans have facial motor cortices that are thicker and richer in local circuitry, and their facial movements have the highest degree of dependency from the primary motor cortex. Finally, great apes and humans have more pronounced direct cortico-facial projections (Sherwood et al. 2004, Dobson and Sherwood, 2011). The facial muscular system consists of a flat web of muscular fascicles, embedded in a variable matrix of connective tissue, and packed into a small two-dimensional matrix under the facial skin. In humans, the 17 paired mimetic (from the Greek “mimesis”, imitation) facial muscles are innervated by the facial nerve, and have their distinct embryological origin from the second branchial arch (for a review, see Cattaneo and Pavesi, 2014). Mimetic facial muscles are believed to lack muscle spindles (Stal, 1994), which may reflect the absence of external loads, and imply an absence of stretch reflexes. Thus, the central nervous system has to process sensory information from the skin receptors in order to infer information on facial movements. Converging evidence suggest that the functional units of the facial muscular system are not represented – as conventionally defined – by the single facial muscle, but rather correspond to smaller bundles of myofibers, each with its own anatomical signature and function (Cattaneo and Pavesi, 2014). John Wiley & Sons 3 This article is protected by copyright. All rights reserved. Journal of Comparative Neurology Page 6 of 23 Facial movements can be categorized in voluntary movements, which are coordinated by cortical pathways, in reflexive movements, and in movements driven by central pattern generators, which are mainly located in the brainstem (Gothard, 2014). Historical aspects Duchenne de Boulogne (1806-1875) was a French neurologist and physiologist, who was fascinated by the mechanisms controlling human facial expressions. Believing that “l’âme est donc la source de l’expression” (the soul is the source of the facial expression), he studied facial muscular action using galvanic stimulation (Duchenne de Boulogne, 1862, see Figure 1). He identified 33 different expressions, including the “Duchenne smile” (Ekman et al., 1990), and proposed a new nomenclature of the facial muscles, suggesting that there is a specific facial muscle for the expression of each emotion. Duchenne's ideas also influenced Charles Darwin’s book “The expression of the emotions in man and animals” (Darwin, 1872). Figure 1 about here The different patterns of facial palsy resulting from central or peripheral lesions of the facial innervation were already described in the textbooks of neurology of the 19th century (e.g., von Strümpell, 1884; Mills, 1898). The clinical observation that a hemispheric stroke involving the territory of the middle cerebral artery results in a paralysis of the contralateral lower face, but spares the upper face, was explained by a bilateral innervation of the upper face, and a unilateral, contralateral innervation of the lower face from the primary motor cortex. Jackson (1884) speculated that unilateral movements, such as limb movements and lower face movements, were rather voluntary movements (and thus more vulnerable to damage), whereas bilateral movements, such as movements of the upper face, were less vulnerable to damage because they belonged to a class of rather automatic movements (as cited in Morecraft et al., 2004). Furthermore, Bechterew (1887) and Nothnagel (1889) speculated in their work about the anatomical basis of the striking clinical observation of the dissociation between voluntary and emotional facial innervation after brain lesions. Human and animal studies John Wiley & Sons 4 This article is protected by copyright. All rights reserved. Page 7 of 23 Journal of Comparative Neurology The anatomical organization of the facial nucleus has been elucidated in both primates and humans (Kuypers, 1958a, 1958b; Jenny and Saper, 1987; Sadota et al. 1987; Welt and Abbs 1990; Van der Werf et al. 1998; Morecraft et al., 2001). Histologically, at least four distinct subnuclei are defined (medial, lateral, dorsolateral, and intermediate subnucleus; Kuypers, 1958a; Jenny and Saper, 1987). The facial subnuclei structure presents similarities between primates and humans (Kuypers, 1958a; Jenny and Saper, 1987). The musculotopic pattern is well preserved across mammals and primates, including humans (Sherwood, 2005). Neurons innervating the same facial muscle are arranged together in longitudinal columns, which are oriented cranio-caudally (see Figure 2B; after Morecraft et al., 2001). Figure 2A and B about here According to Holstege (2002), the dorsal subgroup of the facial nucleus contains motor neurons innervating the muscles around the eye, and the medial subgroup innervates the muscles of the ear. In humans, this latter group is small, since there is a lack of ear musculature. The opposite is found for the lateral subgroup, which is the largest in humans. This subgroup innervates the muscles of the mouth, which are very well developed in humans. It appears that the dorsal portion of the lateral subgroup innervates the muscles of the upper mouth, whereas its ventral portion innervates the muscles of the lower mouth. Thus, for smiling, the motor neurons responsible for the innervation of the upper mouth, in the dorsal portion, would be activated. Conversely, for negative facial expressions, the ventral portion of the lateral facial subgroup might be more important (Holstege, 2002). Sherwood et al. (2005) studied the evolution of the brainstem orofacial motor system in 47 species of primates. They found that hominids present significantly larger volumes of the facial nucleus than predicted. The authors suggest that the phylogenetic specialization of the facial nucleus may be related to the variation
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